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Research article2021Peer reviewedOpen access

Reprogramming of RNA silencing triggered by cucumber mosaic virus infection in Arabidopsis

Annacondia, Maria Luz; Martinez, German

Abstract

Background RNA silencing has an important role mediating sequence-specific virus resistance in plants. The complex interaction of viruses with RNA silencing involves the loading of viral small interfering RNAs (vsiRNAs) into its host ARGONAUTE (AGO) proteins. As a side effect of their antiviral activity, vsiRNAs loading into AGO proteins can also mediate the silencing of endogenous genes. Here, we analyze at the genome-wide level both aspects of the interference of cucumber mosaic virus (CMV) with the RNA silencing machinery of Arabidopsis thaliana. Results We observe CMV-derived vsiRNAs affect the levels of endogenous sRNA classes. Furthermore, we analyze the incorporation of vsiRNAs into AGO proteins with a described antiviral role and the viral suppressor of RNA silencing (VSR) 2b, by combining protein immunoprecipitation with sRNA high-throughput sequencing. Interestingly, vsiRNAs represent a substantial percentage of AGO-loaded sRNAs and displace other endogenous sRNAs. As a countermeasure, the VSR 2b loaded vsiRNAs and mRNA-derived siRNAs, which affect the expression of the genes they derive from. Additionally, we analyze how vsiRNAs incorporate into the endogenous RNA silencing pathways by exploring their target mRNAs using parallel analysis of RNA end (PARE) sequencing, which allow us to identify vsiRNA-targeted genes genome-wide. Conclusions This work exemplifies the complex relationship of RNA viruses with the endogenous RNA silencing machinery and the multiple aspects of virus resistance and virulence that this interaction induces.

Keywords

RNA silencing; Virus; Argonaute; Immunoprecipitation; Cucumber mosaic virus

Published in

Genome Biology
2021, Volume: 22, number: 1, article number: 340
Publisher: BMC

      SLU Authors

      • Associated SLU-program

      SLU Plant Protection Network
      AMR: Virus

      UKÄ Subject classification

      Plant Biotechnology

      Publication identifier

      DOI: https://doi.org/10.1186/s13059-021-02564-z

      Permanent link to this page (URI)

      https://res.slu.se/id/publ/115057